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Wide spread incidences of vaccine-like strains of lumpy skin disease virus (LSDV) have recently been reported in a Russian region with a neighboring country that actively vaccinate with a live attenuated LSD vaccine. The use of live-attenuated viruses (LAVs) as vaccines during an active outbreak, creates potential ground for coinfection of hosts and emergence of a strain combining genetic fragments of both parental vaccine and field strains. In this study, we analyse the vaccine-like strain LSDV RUSSIA/Saratov/2017 detected in Saratovskaya oblast, a region sharing border with Kazakhstan. To gain insight into possible recombination signals, a full-genome next-generation sequencing of the viral genome was performed using the Illumina platform. The genome contains the backbone of a live-attenuated vaccine with a patchwork of wild-type field virus DNA fragments located throughout. A total of 27 recombination events were identified. The average distance between the recombination sites was 3400 base pairs (bp). The impact of the recombination events on the virulence and transmission capacity of the identified virus remains to be clarified. These findings provide evidence for the first time of genetic exchanges between closely related strains of capripoxviruses in the field and a vaccine strain, and prompt a revisiting of the vaccination issue for a safe and efficacious prevention and control strategy of LSD.

In 2015, the lumpy skin disease virus spread throughout the Russian Federation. Following a modified stamping-out campaign, the disease re-emerged with a greater incidence across 16 regions of Southern and Central Russia. A total of 313 outbreaks were reported to OIE. The highest outbreak frequency was observed in the republics of Chechnya (108), Kalmykiya (57), and Ingushetiya (35). The disease cases predominantly occurred in June and July 2016, starting from May to December; however, no association between outbreaks and altitudes was identified (p > .05). Samples taken from infected cattle were subjected to PCR analysis, which identified the genome of the virus most frequently in skin nodules (78%), nasal swabs (23.4%), blood (13%) and sera (14.5%). Interestingly, LSDV genome was occasionally identified in lung and milk samples. Based on the PRO30 sequence analysis, lumpy skin disease virus (LSDV) strains circulating in Russia were all identical and fell within the cluster of field LSDV found worldwide.

Vaccination against lumpy skin disease (LSD) is crucial for maintaining the health of animals and the economic sustainability of farming. Either homologous vaccines consisting of live attenuated LSD virus (LSDV) or heterologous vaccines consisting of live attenuated sheeppox or goatpox virus (SPPV/GPPV) can be used for control of LSDV. Although SPPV/ GTPV-based vaccines exhibit slightly lower efficacy than live attenuated LSDV vaccines, they do not cause vaccine-induced viremia, fever, and clinical symptoms of the disease following vaccination, caused by the replication capacity of live attenuated LSDVs. Recombination of capripoxviruses in the field was a long-standing hypothesis until a naturally occurring recombinant LSDV vaccine isolate was detected in Russia, where the sheeppox vaccine alone is used. This occurred after the initiation of vaccination campaigns using LSDV vaccines in the neighboring countries in 2017, when the first cases of presumed vaccine-like isolate circulation were documented with concurrent detection of a recombinant vaccine isolate in the field. The follow-up findings presented herein show that during the period from 2015 to 2018, the molecular epidemiology of LSDV in Russia split into two independent waves. The 2015-2016 epidemic was attributable to the field isolate. Whereas the 2017 epidemic and, in particular, the 2018 epidemic represented novel disease importations that were not genetically linked to the 2015-2016 field-type incursions. This demonstrated a new emergence rather than the continuation of the field-type epidemic. Since recombinant vaccine-like LSDV isolates appear to have entrenched across the country's border, the policy of using certain live vaccines requires revision in the context of the biosafety threat it presents.

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Since 2012, lumpy skin disease virus (LSDV) has been spreading from the Middle East to south-east Europe and Russia. Although vaccination campaigns have managed to contain LSDV outbreaks, the risk of further spread is still high. The most likely route of LSDV transmission in short distance spread is vector-borne. Several arthropod species have been suggested as potential vectors, but no proven vector has yet been identified. To check whether promiscuous-landing synanthropic flies such as the common housefly (Musca domestica) could be involved, we carried out entomological trapping at the site of a recent LSDV outbreak caused by a vaccine-like LSDV strain. The presence of vaccine-like LSDV DNA was confirmed by the assay developed herein, the assay by Agianniotaki et al. (2017) and RPO30 gene sequencing. No evidence of field LSDV strain circulation was revealed. In this study, we discovered that M. domestica flies carried vaccine-like LSDV DNA (C > 25.5), whereas trapped stable flies from the same collection were negative for both field and vaccine LSDV. To check whether flies were contaminated internally and externally, 50 randomly selected flies from the same collection were washed four times and tested. Viral DNA was mainly detected in the 1st wash fluid, suggesting genome or even viral contamination on the insect cadaver. In this study, internal contamination in the insect bodies without differentiation between the body locations was also revealed; however, the clinical relevance for mechanical transmission is unknown. Further work is needed to clarify a role of M. domestica in the transmission of LSDV. To our knowledge, this is the first report demonstrating that an attenuated LSD vaccine strain has been identified in Russian cattle given the ban on the use of live attenuated vaccines against LSDV.

Summary Lumpy skin disease (LSD) has recently expanded its range northwards to include the Balkans, Turkey and Russia. Because there was no solid evidence conclusively verifying the transmission mechanism in the field and LSDV viraemic animals with overt and asymptomatic presentation of disease and their products may represent a risk as an indirect transmission pathway. In this work, we used PCR positivity and infectivity in clinical and subclinical infection to evaluate the safety of meat and offal products from cows infected with the virulent LSDV strain Russia/Dagestan/2015. At day 21 post infection, seven of the 12 animals developed the generalized disease, and four animals became subclinically infected without apparent clinical signs. Upon examination and necropsy, the animals with the generalized disease had skin lesions; noticeably enlarged lymph nodes; and lesions in the lungs, trachea and testicles; whereas subclinically ill animals exhibited only enlarged lymph nodes and fever. For both disease presentations, testing of skeletal meat by PCR and virus isolation showed that the skeletal meat did not contain live virus or viral genome, whereas in cattle with generalized disease, meat with gross pathology physically connected under the site of a skin lesion was positive for the live virus. In subclinical infection, only enlarged lymph nodes carried the infectious virus, while the other internal organs tested in both types of disease manifestation were negative except for the testicles. Overall, our findings demonstrate that clinically and subclinically infected animals are reservoirs of live LSDV in lymph nodes and testicles, whereas deep skeletal meat in both types of infection do not carry live virus and the risk of transmission through this product seems very low. The detection of LSDV in testicular tissues in subclinically ill animals is concerning because of the potential to spread infection through contaminated semen. This aspect requires reconsideration of surveillance programmes to identify these Trojan horses of LSDV infection.

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